Original article
Chromosomal analysis of the eggs
and ovaries of the laying workers of Apis cerana F
S Verma A Karol
Nimachal Pradesh
University, Department of Bio-Sciences, Summerhill, Shimla-171 005,
(Received
18 March 1991;
HP India
accepted 4 May 1992)
Summary — The chromosomal behavior during mitotic and meiotic cell division of eggs and ovaries of Apis cerana F laying workers has been examined. The laying workers are diploid (2n 32),
but undergo meiosis to produce drone brood which possesses a haploid (n
16) set of chromo=
=
somes.
Apis cerana / meiosis / chromosome number / parthenogenesis / laying worker
INTRODUCTION
In a normal honey bee colony the worker
bees and the queen bee are diploid females but the drones are haploid males.
The ovaries of the queen bee are well
developed and functional, whereas the
ovaries of the worker bees are rudimentary structures and are non-functional.
A number of studies have reported the
unusual occurrence in certain races of
honey bees of impaternate females
among the male progeny of virgin queens
and laying workers. Among the different
races of Apis mellifera F the phenomenon
of female parthenogenesis is most remarkable in Apis mellifera capensis. Onion (1912) reported that worker bees in
the queenless colonies of the capensis
bee start developing ovaries and also possess a developed spermatheca which is
devoid of any kind of sperm cells. Ruttner
(1976) gave an detailed account of capensis taxonomy and concluded that the
workers’ ovaries possess a large number
of ovarioles, that they were also surrounded by a ’court of bees’, and that their
brood was scattered on the comb. Ruttner
obtained several generations of capensis
worker bees without any kind of sexual
mating and suggested that an automictic
type of parthenogenesis took place. Later,
Ruttner and Verma (1983) studied the actual cytological mechanisms of female
parthenogenesis in this race of honey
bees.
A similar phenomenon of female parthenogenesis has been observed in Apis
cerana F (Tokuda, 1924; Akahira and
Sakagami, 1958; Naim et al, 1985). However, no previous attempts have been
made to study the cytological mecha-
nisms involved in female parthenogenesis
of this species of honey bees.
The aim of the present investigation
to make a detailed chromosomal analysis of the ovaries and eggs of the laying
workers of Apis cerana F to determine
how the arrhenotokous production of the
drone brood by the laying worker bees
takes place without any sexual mating.
was
MATERIAL AND METHODS
The laying workers of Apis cerana indica were
obtained from the colonies kept at the Summerhill, Shimla apiary. They were observed about 2
weeks after dequeening. Up to 12 eggs were
found per cell. The eggs were collected with a
fine brush, and the ovaries and eggs were processed for chromosomal preparations. They
were fixed in Carnoy’s fixative (Darlington and
LaCour, 1976). The squash preparations were
stained in acetocarmine (Kitzmiller and Clerk,
1952). The photomicrographs were taken at 90
x 10 magnification.
RESULTS
Each of the 2 ovaries possesses 2-12
ovarioles with 4—5 developing follicles in
each ovariole (fig 1).The mitotically dividing oogonial cells possess 32 chromosomes (fig 2). Some of the meiotic stages
which were observed in the eggs clearly
showed the pairing and recombination of
chromosomes. In diakinesis and metaphase I (figs 3, 4), 16 bivalents were clearly counted. In anaphase I (fig 5), the 2 sets
of chromosomes separated and moved towards opposite poles. The metaphase II
stage of meiosis showed 16 (that is a haploid set) of chromosomes (fig 6). However,
in some of the egg cells the number of bivalents amounted to 8 (fig 7).
DISCUSSION
Apis mellifera capensis (Ruttner,
1976), Apis cerana indica also has laying
workers (Toluda, 1924). In Apis cerana indica the laying worker bee possesses a
pair of ovaries, each ovary consisting of 212 ovarioles with 4-5 developing ova in
each ovariole. Kapil (1962) also reported
the same number of ovarioles in the laying
As in
workers of this bee species. However,
Sato et al (1984) observed 4-9 ovarioles in
the ovaries of Apis cerana japonica laying
workers.
The
oogonial cells of the ovaries of the
workers
of Apis cerana indica have
laying
32 chromosomes (fig 2), as reported in the
queen bee and the other worker bees of
this species (Fahrenhorst, 1977; Verma,
1988). The karyological study of the honey
bee carried out by Hoshiba
ther supports this view.
et al (1978) fur-
The studies performed on the eggs and
ovaries of the laying workers of this bee
showed meiosis. In diakinesis and metaphase I (figs 3, 4) 16 bivalents were found.
This showed the pairing and recombination
of the somatic chromosomes like those of
the laying workers of Apis mellifera capensis (Ruttner and Verma, 1983). The hap-
paire d’ovaires renfermant chacun 2 à
12 ovarioles (fig 1). Dans les préparations
de chromosomes provenant des ovaires
on a trouvé le nombre diploïde de chromosomes, 2n = 32 (fig 2). Ce n’est que dans
les oeufs qu’on a trouvé diverses phases
de la méiose. Aux stades diacinèse et métaphase I, on a observé 16 chromosomes
bivalents (figs 3 et 4). La présence de bivalents montre qu’il existe un appariement et
une nouvelle répartition des chromosomes
homologues. À l’anaphase I (fig 5), les 2
ensembles de chromosomes, comprenant
chacun 16 chromosomes, se déplacent en
direction du pôle opposé. Au stade métaphase II (fig 6) on a également observé
16 chromosol’ensemble haploïde de n
une
loid set of chromosomes formed as a result of meiosis (fig 6) seems to form the
drones chromosomal complement as such
without any type of union because the
same number of chromosomes have also
been found in the drones.
The presence of 8 bivalents (fig 7),
which have been found in many cells, is
an unusual feature. This can be accounted
for by the partial or incomplete pairing of
the 16 bivalents to form tetravalents. A
secondary chromosomal pairing has been
reported during meiotic prophase in Apis
mellifera (Nachtsheim, 1913) and in Apis
mellifera ligustica (Kerr and Silveira,
1972).
The secondary pairing may be due to
the homology among the somatic chromosomes. Deodikar and Thakar (1966) have
reported the probable origin of n 16 from
the 4 heterologous chromosomes, which
may give rise to the homology of the somatic chromosomes. However, this fact
needs further clarification.
=
Résumé — Analyse des chromosomes
des œufs et des ovaires des ouvrières
pondeuses d’Apis cerana F. Les ouvrières
pondeuses d’Apis
cerana
possèdent
=
cellules ne présentaient
que 8 bivalents (fig 7). L’observation de ce
comportement inhabituel des chromosomes nécessite une clarification ultérieure.
mes.
Quelques
Apis cerana/ méiose / parthénogenèse /
nombre de chromosomes / ouvrière
pondeuse
der Chroder Eier und Ovarien von legenden Arbeitsbienen von Apis cerana
F. Die legenden Arbeiterinnen von
A cerana verfügen über ein Paar Ovarien
mit je 2-12 Ovariolen (Abb 1).In den Chromosomenpräparaten aus den Ovarien und
Eiern wurde in den Ovarien die diploide
Zusammenfassug — Analyse
mosomen
Chromosomenzahl, 2n
=
32, gefunden
(Abb 2). Nur in den Eiern wurden verschiedene Stadien der Meiose gefunden. In den
Diakinese- und Metaphase I-Stadien
wurden 16 Bivalente beobachtet (Abb 3
und 4). Das Vorhandensein von Bivalenten
zeigt, daß eine Paarung und Neuverteilung
der homologen Chromosomen erfolgt.
In der Anaphase I (Abb 5) bewegen sich
die beiden Chromosomensätze, jeder mit
16 Chromosomen, in Richtung der entge-
gengesetzten Pole. Auch im Stadium der
II
Metaphase (Abb 6) wurde der haploide
Chromosomensatz von n = 16 festgestellt.
In einigen Zellen waren sogar nur acht
Bivalente zu sehen (Abb 7). Diese Beobachtung eines ungewöhnlichen Verhaltens
der Chromosomen bedarf jedoch noch
weiterer Klärung.
Kerr WE, Silveira ZV (1972) Karyotypic evolution of the bees and corresponding taxonomic implications. Evolution 26, 197-202
Kitzmiller JB, Clark GL (1952) Salivary gland
chromosomes in Culex mosquito. Genetics
37,36
Nachtsheim H (1913) Cytologische Studien über
die Geschlechtsbestimmung bei der Honigbiene (A mellifera L). Arch Zellforsch 11, 170239
Apis cerana / Meiose / Chromosomenzahl / Parthenogenese / legende Arbeitsbiene
Naim M, Phadke KG, Rao PJ (1985) Morphometrics and some behavioural species of
Apis cerana indica workers under queenless
colony condition. Indian J Entomol 47, 179192
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